Elucidating patterns of population structure for species with complex life histories, and disentangling the processes driving such patterns, remains a significant analytical challenge. Humpback whale (Megaptera novaeangliae) populations display complex genetic structures that have not been fully resolved at all spatial scales. We generated a data set of nuclear markers for 3,575 samples spanning the seven breeding stocks and substocks found in the South Atlantic and western and northern Indian Oceans. For the total sample, and males and females separately, we assessed genetic diversity, tested for genetic differentiation between putative populations and isolation by distance, estimated the number of genetic clusters without a priori population information, and estimated rates of gene flow using maximum likelihood and Bayesian approaches. At the ocean basin scale, structure is governed by geographic distance (IBD p<0.05) and female fidelity to breeding areas, in line with current understanding of the drivers of broad-scale population structure. Consistent with previous studies, the Arabian Sea breeding stock was highly genetically differentiated (FST 0.034-0.161; p<0.01 for all comparisons). However, the breeding stock boundary between west South Africa and east Africa was more porous than expected based on genetic differentiation, cluster, and gene flow analyses. Instances of male-fidelity to breeding areas and relatively high rates of dispersal for females were also observed between the three substocks in the western Indian Ocean. This mismatch between demographic units and current management boundaries may have ramifications for assessments of the status and continued protections of populations still in recovery from commercial whaling.